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Ultrasound Obstet Gynecol 2013; 42: 434439

Published online 2 September 2013 in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/uog.12492

Fetoscopic laser ablation of placental anastomoses in


twintwin transfusion syndrome using Solomon technique
R. RUANO*, C. RODO, J. L. PEIRO, A. A. SHAMSHIRSAZ*, S. HAERI*, M. L. NOMURA,
E. M. A. SALUSTIANO, K. K. DE ANDRADE, H. SANGI-HAGHPEYKAR*, E. CARRERAS and
M. A. BELFORT*
*Baylor College of Medicine and Texas Childrens Hospital, Department of Obstetics and Gynecology, Division of Maternal-Fetal
Medicine, Houston, TX, USA; Faculdade de Medicina da Universidade de Sao Paulo, Department of Obstetrics and Gynecology, Sao
Paulo, SP, Brazil; Hospital Universitari Vall dHebron and University Autonoma de Barcelona, Fetal Surgery Program, Barcelona, Spain;
Maternal-Fetal Institute in Campinas, Campinas, Brazil

K E Y W O R D S: fetal surgery; fetoscopy; laser ablation; monochorionic twin pregnancy; twin anemiapolycythemia sequence;
twin oligopolyhydramnios sequence; twintwin transfusion syndrome

ABSTRACT Conclusions Use of the Solomon technique following


selective laser coagulation of placental anastomoses
Objective To document perinatal outcomes following use
appears to improve twin survival and may reduce the risk
of the Solomon technique in the selective photocoag-
of recurrent TTTS and TAPS. Our data support the idea
ulation of placental anastomoses for severe twintwin
of performing a randomized controlled trial to evaluate
transfusion syndrome (TTTS). the effectiveness of the Solomon technique. Copyright
Methods Between January 2010 and July 2012, data 2013 ISUOG. Published by John Wiley & Sons Ltd.
were collected from 102 consecutive monochorionic
twin pregnancies complicated by severe TTTS that INTRODUCTION
underwent fetoscopic laser ablation at four different
centers. We compared outcomes between subjects that Monochorionicdiamniotic twin pregnancies account for
underwent selective laser coagulation using the Solomon 20% of spontaneous twin pregnancies and almost 5% of
technique (cases) and those that underwent selective laser medically assisted twin pregnancies, and approximately
coagulation without this procedure (controls). 1520% of monochorionicdiamniotic twin pregnan-
cies are complicated by twintwin transfusion syndrome
Results Of the 102 pregnancies examined, 26 (25.5%) (TTTS)1,2 . The natural history of (untreated) TTTS is
underwent the Solomon technique and 76 (74.5%) did associated with perinatal death in 90% of cases and neu-
not. Of the 204 fetuses, 139 (68.1%) survived up to 30 rological impairment in 50% of survivors2 . Fetoscopic
days of age. At least one twin survived in 82 (80.4%) laser ablation (FLA) of the superficial placental anas-
pregnancies and both twins survived in 57 (55.9%) tomoses has been considered the standard of care for
pregnancies. When compared with the control group, severe TTTS, with most groups reporting survival of at
the Solomon-technique group had a significantly higher least one twin in 8090% of cases and a 35% rate of
survival rate for both twins (84.6 vs 46.1%; P < 0.01) and neurological impairment among survivors after prenatal
a higher overall neonatal survival rate (45/52 (86.5%) treatment3 6 . Dual survival (i.e. survival of both recipi-
vs 94/152 (61.8%); P < 0.01). Use of the Solomon ent and donor), however, remains lower, at approximately
technique remained independently associated with dual 50%7 9 .
twin survival (adjusted odds ratio (aOR), 11.35 (95% CI, Since the initial studies reporting FLA, different
3.1153.14); P = 0.0007) and overall neonatal survival surgical techniques have been proposed for carrying
rate (aOR, 4.65 (95% CI, 1.5913.62); P = 0.005) on it out3,9 13 . Initially, non-selective laser coagulation of
multivariable analysis. There were no cases of recurrent placental vessels was performed, in which any vessels that
TTTS or twin anemiapolycythemia sequence (TAPS) in crossed the intertwin membranes (membranous equator)
the Solomon-technique group. were coagulated3,10,11 . Selective laser coagulation of

Corresponding to: Dr R. Ruano, Pavilion for Women Texas Childrens Fetal Center, 6651 Main Street, Suite F1020, Houston, TX 77030,
USA (e-mail: Ruano@bcm.edu or rodrigoruano@hotmail.com)
Accepted: 17 April 2013

Copyright 2013 ISUOG. Published by John Wiley & Sons Ltd. ORIGINAL PAPER
Fetoscopic laser ablation with Solomon technique 435

placental vessels (SLCPV) was subsequently reported, in Recipient sac Intertwin membranes
which anastomoses crossing between the twins (vascular
equator) were identified and coagulated12 . Recently,
Chalouhi et al.9,14 proposed performing an SLCPV
Laser fiber
procedure with subsequent surface coagulation of the
placenta between the ablated anastomotic sites in order VA
to create a physical separation of the donors and
the recipients vascular territories on the surface of AA
the placenta. This surgical procedure is known as AV
Solomonization or the Solomon technique. It has
been stated that performing the Solomon technique after
VA
SLCPV may reduce the recurrence of TTTS and/or
the incidence of twin anemiapolycythemia sequence
(TAPS) by coagulating microanastomoses that were not AV
coagulated during the selective laser ablation alone.
However, there are as yet no data in the literature
evaluating this hypothesis. Recipient sac Intertwin membranes
Our aim was to evaluate perinatal outcomes following
use of the Solomon technique in selective photocoagula- Solomonization
tion of placental anastomoses for severe TTTS.

VA
METHODS AA

This was a retrospective study in which data were col- AV


lected from 102 consecutive monochorionicdiamniotic
VA
pregnancies complicated by TTTS that had undergone
FLA in four regional referral centers (Barcelona, Catalo- AV
nia, Spain; Part City, UT and Houston, TX, USA; and
Sao Paulo, Brazil) between January 2010 and July 2012.
Included in the study were pregnancies undergoing FLA
for severe TTTS (Quintero Stages IIIV) performed by
E.C. in Spain, M.A.B. in USA or R.R. in Brazil and USA.
Figure 1 Schematic representation of selective photocoagulation of
All operators had performed FLA in at least 60 cases prior superficial placental anastomoses without (a) and with (b)
to this study and were regarded as experienced. Triplet subsequent use of the Solomon technique. AA, arterioarterial
pregnancies were excluded. The local institutional review anastomosis; AV, arteriovenous anastomosis; VA, venoarterial
boards approved the study. anastomosis.
The two techniques evaluated were SLCPV with
and without use of the Solomon technique (Figure Barcelona, the Solomon technique was not performed
1). All patients underwent a comprehensive ultrasound at all.
evaluation for confirmation of the diagnosis of TTTS and The primary outcome of interest was singleton or twin
establishment of the Quintero stage. In this study, SLCPV survival at 30 days of age. The secondary outcomes
was performed by direct ultrasound-guided uterine entry of interest were occurrence of TAPS and recurrent
with local anesthesia. Using semi-rigid fetoscopes and TTTS. TAPS was diagnosed when antenatal Doppler
an Nd:YAG (Smartpil, Deka, Calenzano, Florence, Italy) ultrasonography revealed a peak systolic velocity in the
or Diode (Multibeam, Dornier Medtech, Kennesaw, GA, middle cerebral artery >1.5 multiples of the median
USA) laser at a power setting of 3045 W, a selective (MoM) in one twin (anemic fetus) and a peak systolic
photocoagulation technique was used to ablate the velocity < 1.0 MoM in the polycythemic twin, in addition
anastomotic vessels after such vessels had been mapped to the postnatal confirmation of an intertwin hemoglobin
by direct visualization. For those cases in which the difference of greater than 8 g/dL15 .
Solomon technique was used, SLCPV was followed by
laser coagulation of the superficial placental surface Statistical analysis
between the anastomoses, creating a line in the vascular
equator and separating the placental territories of the Statistical analysis was performed using IBM SPSS
twins. In all cases, at the conclusion of the procedure, for Windows version 20 (IBM Inc., Armonk, NY,
amniotic fluid in the recipient amniotic cavity was drained USA). Fishers exact test, the chi-square test and
(amnioreduction) in order to achieve a deepest pocket of the MannWhitney U-test were used for comparisons
less than 8 cm. Septostomy was not performed in any case. between groups. Logistic regression analysis was per-
At the two centers in the USA and in Brazil, the Solomon formed to evaluate independent predictors for survival
technique was performed in the most recent cases. In of at least one twin or survival of both twins, with

Copyright 2013 ISUOG. Published by John Wiley & Sons Ltd. Ultrasound Obstet Gynecol 2013; 42: 434439.
436 Ruano et al.

Table 1 Patient characteristics and outcomes after fetoscopic laser ablation of placental anastomoses for severe twintwin transfusion
syndrome (TTTS) with and without use of the Solomon technique

Parameter Solomon technique (n = 26) No Solomon technique (n = 76) P

Maternal age (years) 28.5 (17.041.0) 31.0 (17.040.0) 0.10


Quintero stage 0.19
Stage II 12 (46.2) 38 (50.0)
Stage III 11 (42.3) 36 (47.4)
Stage IV 3 (11.5) 2 (2.6)
Ultrasound intertwin weight discordance (%) 28.0 (5.049.0) 21.0 (0.062.0) 0.19
Gestational age at fetoscopic laser ablation (weeks) 21.0 (16.025.0) 20.0 (15.426.0) 0.19
Location of placenta 0.99
Anterior 11 (42.3) 32 (42.1)
Posterior 15 (57.7) 44 (57.9)
Recurrent TTTS 0 (0.0) 4 (5.3) 0.57
TAPS 0 (0.0) 6 (7.9) 0.33
Iatrogenic septostomy 3 (11.5) 6 (7.9) 0.69
Gestational age at delivery (weeks) 32.0 (16.036.0) 31.2 (16.039.4) 0.68
Intertwin weight discordance at birth (%) 9.5 (4.143.8) 13.0 (3.354.0) 0.49
Survival of at least one twin 23 (88.5) 59 (77.6) 0.27
Survival of both twins 22 (84.6) 35 (46.1) < 0.01

Data shown as median (range) or n (%). TAPS, twin anemiapolycythemia sequence.

Table 2 Patient characteristics and outcomes after fetoscopic laser ablation of placental anastomoses for severe twintwin transfusion
syndrome in cases with at least one survivor 30 days after birth vs those with no survivors

Survival of one or both twins


Parameter (n = 82) No survivors (n = 20) P

Maternal age (years) 31.0 (17.041.0) 29.5 (17.039.0) 0.25


Quintero stage 0.01
Stage II 45 (54.9) 5 (25.0)
Stage III 32 (39.0) 15 (75.0)
Stage IV 5 (6.1) 0 (0.0)
Ultrasound intertwin weight discordance (%) 25.0 (0.062.0) 30.0 (4.060.0) 0.32
Gestational age at fetoscopic laser ablation (weeks) 20.7 (15.926.0) 20.0 (15.423.0) 0.04
Location of placenta 0.08
Anterior 31 (37.8) 12 (60.0)
Posterior 51 (62.2) 8 (40.0)
TAPS 4 (4.9) 2 (10.0) 0.34
Solomon technique 23 (28.0) 3 (15.0) 0.27

Data shown as median (range) or n (%). TAPS, twin anemiapolycythemia sequence.

center of treatment controlled for by including it as a 43 patients; Brazil, 32 patients; USA, 27 patients). All
predictive fixed effect. In the analysis of overall survival, cases treated in Spain underwent selective FLA without the
for which the unit of analysis is each neonate (and there- Solomon technique. In the USA, the Solomon technique
fore n = 204), adjustment for within-pregnancy as well as was performed in 11 patients while selective FLA without
within-center clustering was performed by including both it was performed in 16 cases. In Brazil, 15 patients
variables as random effects in the GLIMMIX procedure underwent FLA with the Solomon technique while 17
in SAS (SAS Institute, Inc., Cary, NC, USA). The GLIM- underwent FLA without it. The median maternal age was
MIX procedure fits generalized linear mixed models and 31.0 (range, 17.041.0) years. Quintero Stages II, III and
estimates the parameters by maximum likelihood. In both IV TTTS were observed in 50 (49.0%), 47 (46.1%) and
logistic regression and generalized linear mixed model five (4.9%) patients, respectively. The median gestational
analysis, adjustment for possible confounders was done age at FLA procedure was 20.0 (range, 15.426.0) weeks
by including these variables in the multivariable regression and median gestational age at delivery was 31.6 (range,
models. P < 0.05 was taken as statistically significant. 16.039.4) weeks. The median intertwin ultrasound-
estimated weight discordance was 25.5 (range, 062)%.
Posterior placenta was observed in 59 patients (57.8%),
RESULTS while anterior placenta was identified in 43 (42.2%) cases.
TAPS and recurrent TTTS were diagnosed in six (5.9%)
A total of 102 monochorionicdiamniotic pregnancies and four (3.9%) patients, respectively. None of the cases
complicated by severe TTTS underwent FLA at the centers of recurrent TTTS required a secondary FLA procedure.
included in this study during the period considered (Spain, A total of 139 (68.1%) infants survived beyond 30 days

Copyright 2013 ISUOG. Published by John Wiley & Sons Ltd. Ultrasound Obstet Gynecol 2013; 42: 434439.
Fetoscopic laser ablation with Solomon technique 437

Table 3 Patient characteristics and outcomes after fetoscopic laser ablation of placental anastomoses for severe twintwin transfusion
syndrome, in cases with survival of both twins 30 days after birth vs those with death of one or both twins

Parameter Survival of both twins (n = 57) One or no survivor (n = 45) P

Maternal age (years) 31.5 (17.041.0) 30.0 (17.040.0) 0.23


Quintero stage 0.09
Stage II 32 (56.1) 18 (40.0)
Stage III 21 (36.8) 26 (57.8)
Stage IV 4 (7.0) 1 (2.2)
Ultrasound intertwin weight discordance (%) 25.5 (4.049.0) 24.0 (0.062.0) 0.79
Gestational age at fetoscopic laser ablation (weeks) 20.7 (15.925.7) 20.0 (15.426.0) 0.68
Location of placenta 0.04
Anterior 19 (33.3) 24 (53.3)
Posterior 38 (66.7) 21 (46.7)
TAPS 3 (5.3) 3 (6.7) 0.99
Solomon technique 22 (38.6) 4 (8.9) < 0.01

Data shown as median (range) or n (%). TAPS, twin anemiapolycythemia sequence.

Table 4 Patient characteristics and outcomes after fetoscopic laser ablation of placental anastomoses for severe twintwin transfusion
syndrome, analyzed per individual twin according to survival 30 days after birth

Parameter Survivors (n = 139) Non-survivors (n = 65) P

Maternal age (years) 30.2 5.5 28.9 5.2 0.22


Quintero stage 0.16
Stage II 77 (55.4) 23 (35.4)
Stage III 53 (38.1) 41 (63.1)
Stage IV 9 (6.5) 1 (1.5)
Ultrasound intertwin weight discordance (%) 22.5 11.0 25.1 16.8 0.36
Gestational age at fetoscopic laser ablation (weeks) 20.5 2.5 20.0 2.4 0.24
Location of placenta 0.03
Anterior 50 (36.0) 36 (55.4)
Posterior 89 (64.0) 29 (44.6)
Solomon technique 45 (32.4) 7 (10.8) < 0.01

Data shown as mean SD or n (%).

of postnatal life. Overall, there was survival of at least least one twins surviving on univariable analysis (odds
one twin in 82 cases (80.4%) and of both twins in 57 ratio (OR), 2.21 (95% CI, 0.6610.09); P = 0.27). On
cases (55.9%). multivariable analysis in a model that contained Quintero
The Solomon technique was performed in 26 pregnan- stage, gestational age at FLA and center of treatment,
cies while SLCPV without the technique was performed the relationship between survival and gestational age
in 76 patients. Table 1 shows the characteristics and at FLA became borderline significant (adjusted OR
outcomes of the patients according to the surgical tech- (aOR), 1.24 (95% CI, 0.991.58); P = 0.07) whereas
nique used. The groups did not differ with respect to lower Quintero stage remained strongly associated with
pregnancy characteristics including maternal age, Quin- survival (Stage II vs higher stage: aOR, 4.16 (95% CI,
tero stage, ultrasound estimated fetal weight discordance, 1.2915.72); P = 0.02). Use of the Solomon technique
gestational age at FLA procedure, location of the placenta remained unrelated to the probability of at least one
and gestational age at birth. Recurrent TTTS and TAPS twins surviving on multivariable analysis (aOR, 2.01
were more frequently seen in the no-Solomon-technique (95% CI, 0.4810.75); P = 0.37).
group (5.3% and 7.9%, respectively) when compared The associations between various variables and sur-
with the Solomon-technique group (0.0% and 0.0%, vival of both twins on univariable analysis is shown in
respectively); however, these differences were not sta- Table 3. Posterior location of the placenta was signifi-
tistically significant (P = 0.57 and P = 0.33, respectively). cantly associated with survival of both twins (P = 0.04)
Iatrogenic septostomy occurred in three cases (11.5%) in and a trend towards statistical significance was seen for
the Solomon-technique group and six cases (7.9%) in the lower Quintero stage (P = 0.09). Use of the Solomon
no-Solomon-technique group (P = 0.69). technique was also associated with increased odds of
Table 2 presents associations on univariable analysis both twins surviving (OR = 6.44 (95% CI, 2.2123.62);
between perinatal factors and survival of at least one P = 0.002). On multivariable analysis with a logistic
twin. The only variables that were statistically associated regression model that included Solomon technique, Quin-
with this outcome were lower Quintero stage (P = 0.01) tero stage, location of the placenta and center of treat-
and higher gestational age at FLA (P = 0.04). Use of the ment, both a posterior location of the placenta (aOR,
Solomon technique was unrelated to the probability of at 2.56 (95% CI, 1.076.36); P = 0.038) and use of the

Copyright 2013 ISUOG. Published by John Wiley & Sons Ltd. Ultrasound Obstet Gynecol 2013; 42: 434439.
438 Ruano et al.

Solomon technique (aOR, 11.35 (95% CI, 3.1153.14); et al.18 reported the SLCPV procedure, in which the
P = 0.0007) remained independently associated with sur- superficial anastomoses are identified initially (mapping),
vival of both twins. Lower Quintero stage showed a with coagulation then performed in this region. According
small positive association with survival of both twins, to Quintero et al., the SLCPV procedure leads to improved
but this did not reach statistical significance on multivari- survival rates of both donor and recipient twins18 . More
able analysis (Stage II vs higher stage: aOR, 2.05 (95% recently, a group from Europe has proposed performing
CI, 0.815.39); P = 0.14). SLCPV followed by the Solomon technique to ensure
Table 4 presents the relationships between perinatal that the entire vascular equator is coagulated9,14 . The
factors and overall neonatal survival on univariable anal- main goal of this technique is to reduce the incidence
ysis. The overall neonatal survival rate was significantly of small, residual anastomoses, thereby reducing rates of
higher among those who underwent the Solomon tech- complications such as recurrent TTTS or TAPS. Our data
nique as compared to those who did not (45/52 (86.5%) suggest that use of the Solomon technique after SLCPV
vs 94/152 (61.8%); OR, 4.46 (95% CI, 1.5412.87); may improve survival rates of both twins and may reduce
P = 0.006) and posterior placental location was also asso- the risk of recurrent TTTS and TAPS. In our series,
ciated with increased odds for survival (OR, 2.33 (95% TAPS occurred only in patients who did not undergo the
CI, 1.075.07); P = 0.03). These associations remained Solomon technique, with a frequency of 7.9%. According
significant on multivariable analysis with adjustment for to the literature, TAPS can occur in 315% of cases after
both within-pregnancy and within-center clustering by fetoscopic laser ablation15,19 22 .
inclusion of these as random effects in a generalized linear Possible complications related to the Solomon tech-
mixed model; the odds for overall survival were over twice nique may include iatrogenic septostomy and asymmetri-
as high with posterior placenta location (vs anterior: aOR, cal placental territory for the twins after dichorionization
2.43 (95% CI, 1.105.39); P = 0.03) and were more than of the placenta. However, we did not observe any signifi-
four and a half times higher when the Solomon technique cant differences between the two groups.
was used as compared with not using this technique (aOR, Our study has some limitations, which merit further
4.65 (95% CI, 1.5913.62); P = 0.005). discussion. Firstly, this was a retrospective analysis and we
therefore relied on the accuracy of our fetal intervention
DISCUSSION datasets for the information presented. Furthermore, not
all cases had postnatal placental pathological analysis,
Our aim was to evaluate perinatal outcomes following and therefore microscopic evaluation of the efficacy of
use of the Solomon technique in addition to SLCPV the Solomon technique could not be undertaken. We
for severe TTTS. Our results suggest that use of the trust that the ongoing randomized clinical trial in Europe
Solomon technique improves the outcome, especially in will address some of these limitations and provide the
double-twin survival (from 46.1% without the Solomon definitive answer as to the effectiveness of the Solomon
technique to 84.6% with it) and also for overall neonatal technique. In addition, the present study had a small
survival (from 61.8% without to 86.5% with the sample size, especially in the Solomon-technique group.
technique). Although the observed difference was not Consequently, the studys power was only 14% for
statistically significant, it is encouraging that there were the outcome at least one twin surviving (88.5% vs
no cases of recurrent TTTS or TAPS in patients who 77.6%), although it was adequately powered (95%) for
underwent the Solomon technique. the outcome both twins surviving (84.6% vs 46.1%),
According to the literature, many centers have been when type I error was set at 0.05 and using a two-sided
performing selective laser coagulation of placental Fishers exact test.
anastomoses without use of the Solomon technique, with In conclusion, this multicenter retrospective cohort
survival rates of at least one infant or both infants of study suggests that SLCPV followed by the Solomon
approximately 80% and 50%, respectively3,9,16 . These technique may afford better double-twin survival than
rates are very similar to our results in the group without SLCPV alone, and that there may be an additional
use of the Solomon technique. Our data, however, beneficial effect in preventing recurrent TTTS and TAPS.
suggest that these rates might be improved by performing Our data support the idea of performing a randomized
the Solomon technique after selective coagulation of controlled trial to evaluate the effectiveness of the
the placental anastomoses, to around 89 and 85%, Solomon technique.
respectively.
Since De Lia et al.10 first described the FLA procedure in
1990, the surgical technique used to identify and coagulate
the superficial anastomoses has undergone numerous
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